Triple-negative/basal-like breast cancer: Clinical, pathologic and molecular features

Expert Review of Anticancer Therapy

Volumn 10, Issue 2, 2010, Pages 199-207

  Venkitaraman, Ramachandran ^a  

^a IPSWICH HOSPITAL NHS TRUST   (United Kingdom)

Author keywords

Basal like breast cancer; BRCA1; Breast; Triple negative breast cancer

Indexed keywords

ANTHRACYCLINE; BEVACIZUMAB; BSI 201; CAPECITABINE; CARBOPLATIN; CETUXIMAB; CYCLOPHOSPHAMIDE; CYLOPHOSPHAMIDE; CYTOKERATIN 5; DASATINIB; DOCETAXEL; DOXORUBICIN; ENZYME INHIBITOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GEFITINIB; GEMCITABINE; IRINOTECAN; IXABEPILONE; LAPATINIB; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; OLAPARIB; PACLITAXEL; PLATINUM DERIVATIVE; PROTEIN INHIBITOR; PROTEIN TYROSINE KINASE INHIBITOR; SELECTIVE ANDROGEN RECEPTOR MODULATOR; SUNITINIB; TAXANE DERIVATIVE; TRABECTEDIN; UNCLASSIFIED DRUG;

ADD ON THERAPY; ADJUVANT CHEMOTHERAPY; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER PATIENT; CANCER RELAPSE; CLINICAL FEATURE; CLINICAL TRIAL; CONTRAST ENHANCEMENT; DNA MICROARRAY; DRUG POTENTIATION; DRUG SENSITIVITY; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; MAMMOGRAPHY; METASTASIS; NUCLEAR MAGNETIC RESONANCE IMAGING; ORAL CONTRACEPTION; OUTCOME ASSESSMENT; PROGNOSIS; REVIEW; RISK FACTOR;

ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; FEMALE; GENE EXPRESSION PROFILING; GENES, BRCA1; HUMANS; RECEPTOR, ERBB-2; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE; RISK FACTORS;

EID: 76749131688     PISSN: 14737140     EISSN: 17448328     Source Type: Journal    
DOI: 10.1586/ERA.09.189     Document Type: Review

References (94)

1. Rakha EA, El-Sayed ME, Green AR, Lee AH, Robertson JF, Ellis IO. Prognostic markers in triple-negative breast cancer. Cancer 109(1), 25-32 (2007).
2. Reis-Filho JS, Tutt AN. Triple negative tumours: a critical review. Histopathology 52(1), 108-118 (2008).
3. Lund MJ, Butler EN, Bumpers HL et al. High prevalence of triple-negative tumors in an urban cancer center. Cancer 113(3), 608-615 (2008).
4. Dolle JM, Daling JR, White E et al. Risk factors for triple-negative breast cancer in women under the age of 45 years. Cancer Epidemiol. Biomarkers Prev. 18(4), 1157-1166 (2009).
5. Millikan RC, Newman B, Tse CK et al. Epidemiology of basal-like breast cancer. Breast Cancer Res. Treat. 109(1), 123-139 (2008).
6. Sorlie T, Tibshirani R, Parker J et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc. Natl Acad. Sci. USA 100(14), 8418-8423 (2003).
7. Sorlie T. Molecular portraits of breast cancer: tumour subtypes as distinct disease entities. Eur. J. Cancer 40(18), 2667-2675 (2004). •• Landmark article describing the molecular subclassification of breastcancers.
8. Rakha EA, Ellis IO. Triple-negative/basal-like breast cancer: review. Pathology 41(1), 40-47 (2009).
9. Chivukula M, Striebel JM, Ersahin C, Dabbs DJ. Evaluation of morphologic features to identify "basal-like phenotype" on core needle biopsies of breast. Appl. Immunohistochem. Mol. Morphol. 16(5), 411-416 (2008).
10. Livasy CA, Karaca G, Nanda R et al. Phenotypic evaluation of the basal-like subtype of invasive breast carcinoma. Mod. Pathol. 19(2), 264-271 (2006).
11. Kreike B, Van Kouwenhove M, Horlings H et al. Gene expression profiling and histopathological characterization of triple-negative/basal-like breast carcinomas. Breast Cancer Res. 9(5), R65 (2007). •• Describes the molecular and histopathologic characterization of triple negative/basal-like breast cancers.
12. Arnes JB, Brunet JS, Stefansson I et al. Placental cadherin and the basal epithelial phenotype of BRCA1-related breast cancer. Clin. Cancer Res. 11(11), 4003-4011 (2005).
13. Bori R, Cserni G. Basal phenotype in breast carcinoma occurring in women aged 35 or younger. Pathol. Oncol. Res. 15(1), 41-45 (2009).
14. Lerma E, Peiro G, Ramon T et al. Immunohistochemical heterogeneity of breast carcinomas negative for estrogen receptors, progesterone receptors and HER2/neu (basal-like breast carcinomas). Mod. Pathol. 20(11), 1200-1207 (2007).
15. Sarrio D, Rodriguez-Pinilla SM, Hardisson D, Cano A, Moreno-Bueno G, Palacios J. Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res. 68(4), 989-997 (2008).
16. Sorlie T, Perou CM, Tibshirani R et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl Acad. Sci. USA 98(19), 10869-10874 (2001).
17. Nielsen TO, Hsu FD, Jensen K et al. Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin. Cancer Res. 10(16), 5367-5374 (2004).
18. Elsheikh SE, Green AR, Rakha EA et al. Caveolin 1 and caveolin 2 are associated with breast cancer basal-like and triple-negative immunophenotype. Br. J. Cancer 99(2), 327-334 (2008).
19. Gauthier ML, Berman HK, Miller C et al. Abrogated response to cellular stress identifies DCIS associated with subsequent tumor events and defines basal-like breast tumors. Cancer Cell 12(5), 479-491 (2007).
20. Tan DS, Marchio C, Jones RL et al. Triple negative breast cancer: molecular profiling and prognostic impact in adjuvant anthracycline-treated patients. Breast Cancer Res. Treat. 111(1), 27-44 (2008).
21. Toyama T, Yamashita H, Kondo N et al. Frequently increased epidermal growth factor receptor (EGFR) copy numbers and decreased BRCA1 mRNA expression in Japanese triple-negative breast cancers. BMC Cancer 8, 309 (2008).
22. Viale G, Rotmensz N, Maisonneuve P et al. Invasive ductal carcinoma of the breast with the "triple-negative" phenotype: prognostic implications of EGFR immunoreactivity. Breast Cancer Res. Treat. 116(2), 317-328 (2009).
23. Bhargava R, Gerald WL, Li AR et al. EGFR gene amplification in breast cancer: Correlation with epidermal growth factor receptor mRNA and protein expression and HER-2 status and absence of EGFR-activating mutations. Mod. Pathol. 18(8), 1027-1033 (2005).
24. Andre F, Job B, Dessen P et al. Molecular characterization of breast cancer with high-resolution oligonucleotide comparative genomic hybridization array. Clin. Cancer Res. 15(2), 441-451 (2009).
25. Bertucci F, Finetti P, Cervera N et al. Howbasal are triple-negative breast cancers? Int. J. Cancer 123(1), 236-240 (2008).
26. Cheang MC, Voduc D, Bajdik C et al. Basal-like breast cancer defined by five biomarkers has superior prognostic value than triple-negative phenotype. Clin. Cancer Res. 14(5), 1368-1376 (2008).
27. Reis-Filho JS, Milanezi F, Steele D et al. Metaplastic breast carcinomas are basal-like tumours. Histopathology 49(1), 10-21 (2006).
28. Bryan BB, Schnitt SJ, Collins LC. Ductalcarcinoma in situ with basal-like phenotype: a possible precursor to invasive basal-like breast cancer. Mod. Pathol. 19(5), 617-621 (2006).
29. Paredes J, Lopes N, Milanezi F, Schmitt FC. P-cadherin and cytokeratin 5: useful adjunct markers to distinguish basal-like ductal carcinomas in situ. Virchows Arch. 450(1), 73-80 (2007).
30. Dabbs DJ, Chivukula M, Carter G, Bhargava R. Basal phenotype of ductal carcinoma in situ: recognition and immunohistologic profile. Mod. Pathol. 19(11), 1506-1511 (2006).
31. Honrado E, Benitez J, Palacios J. Histopathology of BRCA1- and BRCA2-associated breast cancer. Crit. Rev. Oncol. Hematol. 59(1), 27-39 (2006).
32. Lakhani SR, Reis-Filho JS, Fulford L et al. Prediction of BRCA1 status in patients with breast cancer using estrogen receptor and basal phenotype. Clin. Cancer Res. 11(14), 5175-5180 (2005).
33. Foulkes WD, Stefansson IM, Chappuis PO et al. Germline BRCA1 mutations and a basal epithelial phenotype in breast cancer. J. Natl Cancer Inst. 95(19), 1482-1485 (2003). • Describes the relationship between germline BRCA1 mutation and basal-like breast cancers.
34. Rodriguez-Pinilla SM, Sarrio D, Honrado E et al. Vimentin and laminin expression is associated with basal-like phenotype in both sporadic and BRCA1-associated breast carcinomas. J. Clin. Pathol. 60(9), 1006-1012 (2007).
35. Turner NC, Reis-Filho JS, Russell AM et al. BRCA1 dysfunction in sporadic basal-like breast cancer. Oncogene 26(14), 2126-2132 (2007).
36. Turner NC, Reis-Filho JS. Basal-like breast cancer and the BRCA1 phenotype. Oncogene 25(43), 5846-5853 (2006).
37. Atchley DP, Albarracin CT, Lopez A et al. Clinical and pathologic characteristics of patients with BRCA-positive and BRCA-negative breast cancer. J. Clin. Oncol. 26(26), 4282-4288 (2008).
38. Luck AA, Evans AJ, James JJ et al. Breastcarcinoma with basal phenotype: mammographic findings. AJR Am. J. Roentgenol. 191(2), 346-351 (2008).
39. Yang WT, Dryden M, Broglio K et al. Mammographic features of triple receptor-negative primary breast cancers in young premenopausal women. Breast Cancer Res. Treat. 111(3), 405-410 (2008).
40. Collett K, Stefansson IM, Eide J et al. A basal epithelial phenotype is more frequent in interval breast cancers compared with screen detected tumors. Cancer Epidemiol. Biomarkers Prev. 14(5), 1108-1112 (2005).
41. Chen JH, Mehta RS, Carpenter PM, Nalcioglu O, Su MY. Magnetic resonance imaging in predicting pathological response of triple negative breast cancer following neoadjuvant chemotherapy. J. Clin. Oncol. 25(35), 5667-5669 (2007).
42. Uematsu T, Kasami M, Yuen S. Triple-negative breast cancer: correlation between MR imaging and pathologic findings. Radiology 250(3), 638-647 (2009).
43. Basu S, Chen W, Tchou J et al. Comparison of triple-negative and estrogen receptor-positive/progesterone receptor-positive/HER2-negative breast carcinoma using quantitative fluorine-18 fluorodeoxyglucose/positron emission tomography imaging parameters: a potentially useful method for disease characterization. Cancer 112(5), 995-1000 (2008).
44. Gerson R, Alban F, Villalobos A, Serrano A. [Recurrence and survival rates among early breast cancer cases with triple negative immunophenotype]. Gac. Med. Mex. 144(1), 27-34 (2008).
45. Nishimura R, Arima N. Is triple negative a prognostic factor in breast cancer? Breast Cancer 15(4), 303-308 (2008).
46. Haffty BG, Yang Q, Reiss M et al. Locoregional relapse and distant metastasis in conservatively managed triple negative early-stage breast cancer. J. Clin. Oncol. 24(36), 5652-5657 (2006).
47. Dent R, Hanna WM, Trudeau M, Rawlinson E, Sun P, Narod SA. Pattern of metastatic spread in triple-negative breast cancer. Breast Cancer Res. Treat. 115(2), 423-428 (2009).
48. Dent R, Trudeau M, Pritchard KI et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin. Cancer Res. 13(15 Pt 1), 4429-4434 (2007).
49. Dent R, Hanna WM, Trudeau M, Rawlinson E, Sun P, Narod SA. Pattern of metastatic spread in triple-negative breast cancer. Breast Cancer Res. Treat. 115(2), 423-428 (2009).
50. Evans AJ, Rakha EA, Pinder SE, Green AR, Paish C, Ellis IO. Basal phenotype: a powerful prognostic factor in small screen-detected invasive breast cancer with long-term follow-up. J. Med. Screen. 14(4), 210-214 (2007).
51. Bauer KR, Brown M, Cress RD, Parise CA, Caggiano V. Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype: a population-based study from the California cancer registry. Cancer 109(9), 1721-1728 (2007).
52. Rakha EA, El-Rehim DA, Paish C et al. Basal phenotype identifies a poor prognostic subgroup of breast cancer of clinical importance. Eur. J. Cancer 42(18), 3149-3156 (2006).
53. Mulligan AM, Pinnaduwage D, Bull SB, O'Malley FP, Andrulis IL. Prognostic effect of basal-like breast cancers is time dependent: evidence from tissue microarray studies on a lymph node-negative cohort. Clin. Cancer Res. 14(13), 4168-4174 (2008).
54. Tischkowitz M, Brunet JS, Begin LR et al. Use of immunohistochemical markers can refine prognosis in triple negative breast cancer. BMC Cancer 7, 134 (2007).
55. Nofech-Mozes S, Trudeau M, Kahn HK et al. Patterns of recurrence in the basal and non-basal subtypes of triple-negative breast cancers. Breast Cancer Res. Treat. 118(1), 131-137 (2009).
56. Nogi H, Kobayashi T, Suzuki M et al. EGFR as paradoxical predictor of chemosensitivity and outcome among triple-negative breast cancer. Oncol. Rep. 21(2), 413-417 (2009).
57. Fulford LG, Reis-Filho JS, Ryder K et al. Basal-like grade III invasive ductal carcinoma of the breast: patterns of metastasis and long-term survival. Breast Cancer Res. 9(1), R4 (2007).
58. Crabb SJ, Cheang MC, Leung S et al. Basalbreast cancer molecular subtype predicts for lower incidence of axillary lymph node metastases in primary breast cancer. Clin. Breast Cancer 8(3), 249-256 (2008).
59. Liedtke C, Mazouni C, Hess KR et al. Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer. J. Clin. Oncol. 26(8), 1275-1281 (2008).
60. Luck AA, Evans AJ, Green AR, Rakha EA, Paish C, Ellis IO. The influence of basal phenotype on the metastatic pattern of breast cancer. Clin. Oncol. (R. Coll. Radiol.) 20(1), 40-45 (2008).
61. Lin NU, Claus E, Sohl J, Razzak AR, Arnaout A, Winer EP. Sites of distant recurrence and clinical outcomes in patients with metastatic triple-negative breast cancer: high incidence of central nervous system metastases. Cancer 113(10), 2638-2645 (2008).
62. Hines SL, Vallow LA, Tan WW, McNeil RB, Perez EA, Jain A. Clinical outcomes after a diagnosis of brain metastases in patients with estrogen- and/or human epidermal growth factor receptor 2-positive versus triple-negative breast cancer. Ann. Oncol. 19(9), 1561-1565 (2008).
63. Miyoshi Y, Murase K, Oh K. Basal-like subtype and BRCA1 dysfunction in breast cancers. Int. J. Clin. Oncol. 13(5), 395-400 (2008).
64. Carey LA, Dees EC, Sawyer L et al. Thetriple negative paradox: primary tumor chemosensitivity of breast cancer subtypes. Clin. Cancer Res. 13(8), 2329-2334 (2007).
65. Gilmore PM, McCabe N, Quinn JE et al. BRCA1 interacts with and is required for paclitaxel-induced activation of mitogen-activated protein kinase kinase kinase 3. Cancer Res. 64(12), 4148-4154 (2004).
66. Harris LN, Broadwater G, Lin NU et al. Molecular subtypes of breast cancer in relation to paclitaxel response and outcomes in women with metastatic disease: results from CALGB 9342. Breast Cancer Res. 8(6), R66 (2006).
67. Rouzier R, Perou CM, Symmans WF et al. Breast cancer molecular subtypes respond differently to preoperative chemotherapy. Clin. Cancer Res. 11(16), 5678-5685 (2005).
68. Vekris A, Meynard D, Haaz MC, BayssasM, Bonnet J, Robert J. Molecular determinants of the cytotoxicity of platinum compounds: the contribution of in silico research. Cancer Res. 64(1), 356-362 (2004).
69. Leong CO, Vidnovic N, DeYoung MP, Sgroi D, Ellisen LW. The p63/p73 network mediates chemosensitivity to cisplatin in a biologically defined subset of primary breast cancers. J. Clin. Invest. 117(5), 1370-1380 (2007).
70. Sirohi B, Arnedos M, Popat S et al. Platinum-based chemotherapy in triple-negative breast cancer. Ann. Oncol. 19(11), 1847-1852 (2008).
71. Torrisi R, Balduzzi A, Ghisini R et al. Tailored preoperative treatment of locally advanced triple negative (hormone receptor negative and HER2 negative) breast cancer with epirubicin, cisplatin, and infusional fluorouracil followed by weekly paclitaxel. Cancer Chemother. Pharmacol. 62(4), 667-672 (2008).
72. Byrski T, Gronwald J, Huzarski T et al. Response to neo-adjuvant chemotherapy in women with BRCA1-positive breast cancers. Breast Cancer Res. Treat. 108(2), 289-296 (2008).
73. Hayes DF, Thor AD, Dressler LG et al. HER2 and response to paclitaxel in node-positive breast cancer. N. Engl. J. Med. 357(15), 1496-1506 (2007).
74. Gluz O, Nitz UA, Harbeck N et al. Triple-negative high-risk breast cancer derives particular benefit from dose intensification of adjuvant chemotherapy: results of WSG AM-01 trial. Ann. Oncol. 19(5), 861-870 (2008).
75. Citron ML, Berry DA, Cirrincione C et al. Randomized trial of dose-dense versus conventionally scheduled and sequential versus concurrent combination chemotherapy as postoperative adjuvant treatment of node-positive primary breast cancer: first report of intergroup trial c9741/Cancer and Leukemia Group B trial 9741. J. Clin. Oncol. 21(8), 1431-1439 (2003).
76. Diallo-Danebrock R, Ting E, Gluz O et al. Protein expression profiling in high-risk breast cancer patients treated with high-dose or conventional dose-dense chemotherapy. Clin. Cancer Res. 13(2 Pt 1), 488-497 (2007).
77. Nieto Y, Shpall EJ. High-dose chemotherapy for high-risk primary and metastatic breast cancer: is another look warranted? Curr. Opin. Oncol. 21(2), 150-157 (2009).
78. Tan AR, Swain SM. Therapeutic strategies for triple-negative breast cancer. Cancer J. 14(6), 343-351 (2008).
79. Corkery B, Crown J, Clynes M, O'Donovan N. Epidermal growth factor receptor as a potential therapeutic target in triple-negative breast cancer. Ann. Oncol. (2009).
80. Oliveras-Ferraros C, Vazquez-Martin A, Lopez-Bonet E et al. Growth and molecular interactions of the anti-EGFR antibody cetuximab and the DNA cross-linking agent cisplatin in gefitinib-resistant MDA-MB-468 cells: new prospects in the treatment of triple-negative/basal-like breast cancer. Int. J. Oncol. 33(6), 1165-1176 (2008).
81. Bouchalova K, Cizkova M, Cwiertka K, Trojanec R, Hajduch M. Triple negative breast cancer - current status and prospective targeted treatment based on HER1 (EGFR), TOP2A and c-Myc gene assessment. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc. Czech Repub. 153(1), 13-17 (2009).
82. Ribeiro-Silva A, Ribeiro Do Vale F, Zucoloto S. Vascular endothelial growth factor expression in the basal subtype of breast carcinoma. Am. J. Clin. Pathol. 125(4), 512-518 (2006).
83. Miller K, Wang M, Gralow J et al. Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer. N. Engl. J. Med. 357(26), 2666-2676 (2007).
84. Burstein HJ, Elias AD, Rugo HS et al. Phase II study of sunitinib malate, an oral multitargeted tyrosine kinase inhibitor, in patients with metastatic breast cancer previously treated with an anthracycline and a taxane. J. Clin. Oncol. 26(11), 1810-1816 (2008).
85. Rottenberg S, Jaspers JE, Kersbergen A et al. High sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor Azd2281 alone and in combination with platinum drugs. Proc. Natl Acad. Sci. USA 105(44), 17079-17084 (2008).
86. Fong PC, Boss DS, Yap TA et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N. Engl. J. Med. 361(2), 123-134 (2009).
87. O'Shaughnessy JOC, Pippen J. Efficacy of BSI-201, a poly (ADP-ribose) polymerase-1 (PARP1) inhibitor, in combination with gemcitabine/carboplatin (G/C) in patients with metastatic triple-negative breast cancer (TNBC). J. Clin. Oncol. 27(Suppl. 18), (2009) (Abstract 3).
88. Dizdar O, Dede DS, Bulut N, Altundag K. Dasatinib may also inhibit c-kit in triple negative breast cancer cell lines. Breast Cancer Res. Treat. 107(2), 303 (2008).
89. Finn RS. Targeting src in breast cancer. Ann. Oncol. 19(8), 1379-1386 (2008).
90. Huang F, Reeves K, Han X et al. Identification of candidate molecular markers predicting sensitivity in solid tumors to dasatinib: rationale for patient selection. Cancer Res. 67(5), 2226-2238 (2007).
91. Chen Y, Olopade OI. Myc in breast tumor progression. Expert Rev. Anticancer Ther. 8(10), 1689-1698 (2008).
92. Kurebayashi J. Possible treatment strategies for triple-negative breast cancer on the basis of molecular characteristics. Breast Cancer 16(4), 275-280 (2009).
93. Yuli C, Shao N, Rao R et al. BRCA1a has antitumor activity in TN breast, ovarian and prostate cancers. Oncogene 26(41), 6031-6037 (2007).
94. Rahman M, Davis SR, Pumphrey JG et al. TRAIL induces apoptosis in triple-negative breast cancer cells with a mesenchymal phenotype. Breast Cancer Res. Treat. 113(2), 217-230 (2009).